Stable, interactive modulation of neuronal oscillations produced through brain-machine equilibrium.

McNamara CG
Rothwell M
Sharott A

Rhythmic electrical activity is important for brain function. Here, we detected the peak or troughs of such rhythmic activity in real-time and instantly delivered electrical stimulation to the brain. Depending on the timing of stimulation, brain activity and the stimulation pattern became more or less rhythmic simultaneously, demonstrating a stable brain-machine interaction.

Scientific Abstract

Closed-loop interaction has the potential to regulate ongoing brain activity by continuously binding an external stimulation to specific dynamics of a neural circuit. Achieving interactive modulation requires a stable brain-machine feedback loop. Here, we demonstrate that it is possible to maintain oscillatory brain activity in a desired state by delivering stimulation accurately aligned with the timing of each cycle. We develop a fast algorithm that responds on a cycle-by-cycle basis to stimulate basal ganglia nuclei at predetermined phases of successive cortical beta cycles in parkinsonian rats. Using this approach, an equilibrium emerges between the modified brain signal and feedback-dependent stimulation pattern, leading to sustained amplification or suppression of the oscillation depending on the phase targeted. Beta amplification slows movement speed by biasing the animal's mode of locomotion. Together, these findings show that highly responsive, phase-dependent stimulation can achieve a stable brain-machine interaction that leads to robust modulation of ongoing behavior.

Graphical abstract showing schematic descriptions of the main concepts of the paper.
Top panel: Closed-loop electrical stimulation was delivered to the globus pallidus (GPe) at predetermined target phases of the cortical beta oscillation using a fast algorithm that responds on a cycle-by-cycle basis. Middle panel: With stimulation at different target phases, different types of brain-machine equilibrium emerged, whereby the beta oscillation was amplified and stimulation pattern became more regular or the oscillation was suppressed and the stimulation pattern became more variable. Bottom panel: Amplification of beta oscillations slowed movement speed by biasing the animal's mode of locomotion, demonstrating behavioural relevance.

2022. Cell Rep, 41(6):111616.

Related Content
Xie X, Zhang D, Yu T, Duan Y, Daly I, He S

2023. Front Hum Neurosci, 17:1280281.

Torrecillos F, Falato E, Pogosyan A, West TO, Di Lazzaro V, Brown P
2020. J. Neurosci., 40(2):369-381.
He S, Everest-Phillips C, Clouter A, Brown P, Tan H
2020. J. Neurosci., 40(20):4021-4032.